Charles Darwin was baffled by the speed with which flowers evolved and spread. Now genetics could solve the mystery

It was, Charles Darwin wrote in 1879, “an abominable mystery”. Elsewhere he described it as “a most perplexing phenomenon”. Twenty years after the publication of his seminal work The Origin of Species, there were still aspects of evolution that bothered the father of evolutionary biology. Chief among these was the flower problem.

Flowering plants from gardenias to grasses, water lilies to wheat belong to a large and diverse group called the angiosperms. Unlike almost all other types of plants, they produce fruits that contain seeds. What worried Darwin was that the very earliest samples in the fossil record all dated back to the middle of the Cretaceous period, around 100 million years ago, and they came in a bewilderingly wide variety of shapes and sizes. This suggested flowering plants had experienced an explosive burst of diversity very shortly after their origins – which, if true, threatened to undermine Darwin’s entire model of gradual evolution through natural selection.

In fact recently published research has revealed that angiosperms evolved relatively gradually after all. Yet this still leaves a number of key questions. The roughly 350,000 known species of flowering plants make up about 90% of all living plant species. Without them, we would have none of our major crops including those used to feed livestock, and one of the most important carbon sinks that mop up our carbon dioxide emissions would be missing. How and where did they originate? And, perhaps more importantly, why did they become so spectacularly successful?

This 2012 video is about research into the origins of flowering plants.

Darwin was an undoubted expert on origins. His remarkable insights helped establish a framework for the way new species form – and he was adamant that the process was slow and gradual.

“As natural selection acts solely by accumulating slight, successive, favourable variations, it can produce no great or sudden modification; it can act only by very short and slow steps,” he wrote in The Origin of Species.

But Darwin was painfully aware that there were apparent exceptions to his slow and steady rule. The angiosperms were a particular source of frustration. Angiosperms simply didn’t exist for most of Earth’s history. Early forests were populated by bizarre primitive tree-like plants closely related to the club mosses and horsetails that are a very minor part of today’s plant communities. Later a group called the gymnosperms – plants with unenclosed seeds such as the conifers – took over. And then came the angiosperms.

He was well aware the sudden appearance of flowering plants was more than just perplexing. It also provided his critics with ammunition against his evolutionary model.

Darwin did suggest a solution, however. Angiosperms, he said, may have evolved gradually in a remote region of the world as yet unexplored by scientists. By the middle of the Cretaceous, something caused them to spill out of their homeland and rapidly spread across the world. This, reasoned Darwin, would give the misleading impression to researchers working in Europe and North America that a wide variety of flowering plant species had all evolved at the same time. Aware of the lack of evidence to back up his theory, Darwin described it as “wretchedly poor”.

In fact, his speculation has since proved to be partly correct. Angiosperms that predate the middle Cretaceous specimens by tens of millions of years have begun to turn up in rocks from China. But Darwin didn’t get the details entirely right because very rare early angiosperms have been found in Europe and the US too.

“Our knowledge has greatly increased since the end of the 19th century,” says Laurent Augusto at the National Institute for Agricultural Research in Bordeaux, France. Palaeobotanists may not yet agree on precisely where and when flowering plants first evolved, but their appearance in the fossil record much earlier than was previously known means they are no longer a problem for Darwin’s theory of gradual evolution. Other debates about them, especially concerning their spectacular diversity, remain active, however.

“Our world is an angiosperm world,” says Augusto. “In many ecosystems they dominate in species and in biomass – this angiosperm ecological dominance remains unexplained.”

This video from the USA is called Floral Beaks and Flower Evolution.

Clues to the ultimate origins of flowering plants are to be found on New Caledonia, a small island about 1,600 kilometres east of Australia. Here, around the time that Darwin was agonising over his angiosperm problem, botanists discovered a plant called Amborella. Careful study over the last century has shown it to be the sole survivor of one of the very earliest branches of the angiosperm evolutionary tree. This means its relationship to all living flowers is bit like that of the duck-billed platypus to all living mammals: it might look unassuming, but Amborella can tell us more than even the most elaborate orchid about how the angiosperms first evolved.

Last year, the plant finally spilled some of its secrets. The Amborella Genome Project unveiled a draft version of the plant’s genome. The first angiosperms must have evolved from one of the gymnosperm species that dominated the world at the time. The Amborella genome suggests that the first angiosperms probably appeared when the ancestral gymnosperm underwent a ‘whole genome doubling‘ event about 200 million years ago.

Genome doubling occurs when an organism mistakenly gains an extra copy of every one of its genes during the cell division that occurs as part of sexual reproduction. The extra genetic material gives genome doubled organisms the potential to evolve new traits that can provide a competitive advantage. In the case of the earliest angiosperms, the additional genetic material gave the plants the potential to evolve new, never-before-seen structures – like flowers. The world’s flora would never be the same again.

The Amborella genome results strongly suggest that flowers have been a defining feature of the angiosperms from very early on in their evolution. Could the flowers themselves help explain why the angiosperms became so diverse?

Darwin was certainly open to the possibility. While he was wrestling with the problem posed by the seemingly sudden appearance of the angiosperms, he received a letter from Gaston de Saporta, a French biologist who said the apparent evidence of the 19th century fossil record suggesting the plant group appeared suddenly need not be a problem for Darwin’s theory of gradual evolution. It simply showed that angiosperms were an unusual exception to his general rule. Flowering plants and their insect pollinators evolved together, reasoned Saporta, and this ‘co-evolution’ drove both groups to diversify unusually rapidly.

“Your idea … seems to me a splendid one,” responded an enthusiastic Darwin. “I am surprised that the idea never occurred to me, but this is always the case when one first hears a new and simple explanation of some mysterious phenomenon.”

But the theory runs into trouble today, says Augusto. Early angiosperms may have had flowers, but we now know from fossils that those first flowers were very plain – and probably not that attractive to pollinators. By the time the big, bold flowers that entice insects appeared, the angiosperms were already diverse.

Another theory, advanced by Frank Berendse and Marten Scheffer at Wageningen University in the Netherlands in 2009, rests on the fact that the angiosperms are much more productive than gymnosperms like the conifers. Perhaps they simply outcompeted rival plants by growing faster and gobbling up the lion’s share of the nutrients, they suggested.

“Our paper was meant to be a bit provocative,” says Berendse, to encourage botanists and those who study fossil plants to work together more closely on explaining the spectacular rise of the angiosperms.

In fact, the two had already begun working together. Earlier in 2009, a team led by Tim Brodribb at the University of Tasmania in Hobart, Australia, published the first in a series of papers exploring angiosperm evolution by examining fossil leaves. They found that their leaves gained many more veins during the Cretaceous, which would have provided them with more water for photosynthesis, and allowed them to grow more rapidly.

“That provided very strong support for our ideas,” says Berendse. But as with the flower hypothesis, problems remain with the nutrient-based theory. For instance, while individual angiosperm leaves are more efficient at photosynthesising than conifer needles, conifers may be able to compensate because their needles collectively have a much larger surface area than that of the leaves of an average angiosperm tree.

Unfortunately, there are no simple explanations for the diversity and ecological dominance of the flowering plants. “Very probably no single theory can explain the massive rise of the angiosperms,” admits Berendse.

It’s more likely, says Augusto, that several factors played a role, with each being more or less important in specific places and times. For instance, Berendse’s productivity theory may apply in the tropical belts, where rich soils could give nutrient-hungry angiosperms a vital edge over gymnosperms, but it might not explain what’s going on in regions with poor soils, where angiosperms are potentially starved of the nutrients they need. And the simple flowers of early angiosperms may have done little for the evolution of the group, but when elaborate flowers finally appeared they probably did help drive the plant group to take over the world.

That is, if they really did take over the world. It might seem odd to suggest otherwise when there are something like 350,000 known angiosperm species and not many more than 1000 gymnosperms, most of which are conifers. But there’s more to success than diversity, says Brodribb. Many of the few conifers species that do survive are super-abundant.

“In the northern hemisphere conifers rule the vast boreal and much of the temperate zone,” says Brodribb. He adds that the angiosperms have not become ecologically dominant in many of these regions. This might be because the soils there are too poor for them to establish a nutritional advantage, in keeping with Berendse’s ideas, or perhaps it’s because temperatures drop too low for them to survive. But why even in 350,000 attempts the angiosperms haven’t come up with species that can overcome these problems and outcompete those northern conifers is another unsolved mystery.

Today’s plant scientists understandably have a better handle on the origins of flowering plants than Darwin did, but they are still struggling to explain the group’s diversity, and why despite this it has failed to become dominant in some parts of the world.

Augusto, at least, is confident that answers will eventually be found, in part because these mysteries continue to fascinate researchers. And while there is little doubt this fascination stems in part from the ecological and economic importance of angiosperms today, perhaps it is also partly down to Darwin and his way with words. “I think the ‘abominable mystery’ quote does contribute to the general interest in angiosperms,” adds Augusto.

Charles Darwin‘s massive ship library, including astounding drawings of species from far-off lands, meant he rarely had to come above-board while sailing on the Beagle in the 1830s.

Charles Darwin’s five-year journey to and from the Galapagos Islands ended in 1836. While that was over two decades before the publication of On the Origin of Species, he credited his time on board the Beagle as a formative experience for his theory of evolution. That extended trip wasn’t only spent studying local wildlife, especially during lengthy voyages at sea to and from home—Darwin also devoured a library of more than 400 volumes of text.

While many of those books were referenced in his later research, they were not preserved as a collection once the Beagle returned to England, leaving a gap in our understanding about the books and studies that kept Darwin’s mind occupied during such an historic era. Now, thanks to the painstaking efforts of a two-year Beagle project funded by the government of Singapore, that complete on-ship library has been transcribed and posted at Darwin Online, the world’s largest repository of Darwin-related texts and writings.

The library, which was stored in the same cabin as Darwin’s bed and desk during his journey, totaled out at 195,000 pages by the time researchers at the National University of Singapore assembled the full collection (and these weren’t exactly picture books, with only 5,000 corresponding illustrations). The complete list is quite astounding, made up of atlases, history books, geology studies, and even a giant supply of literature. Darwin also enjoyed a few books in French, Spanish, and German, along with a book in Latin about species and a Greek edition of the New Testament.

Despite popular belief birds can have a brilliant plumage, a virtuosic singing chirp and an intricate dance routine say scientists.

The author of a new study, Nick Mason, from the the Cornell Lab of Ornithology in New York state, challenged the long-held notion, first proposed by Charles Darwin, that for a bird species to excel in one area it must give up its edge in another.

For example, male northern cardinals are a dazzling scarlet, but sing a fairly simple whistle, whereas the dull brown House Wren sings one of the most complicated songs in nature.

Mason and his colleagues tested the theory by examining a very large family of songbirds from Central and South America, the tanagers.

This group consists of 371 species and included some of the most spectacularly colourful birds in the world such as the paradise tanager as well as the more drab birds, such the black-bellied seedeater. The group also includes both accomplished and weak songsters alike.

“If there were going to be any group of birds at all that would show this trade-off, the tanagers would be a very good candidate, because there’s all this variation in song and plumage complexity,” Mason said.

“But when we dived into it and did some rigorous statistics, it turns out that there is no overall trend. Tanagers can be drab and plain-sounding, or colourful and musical, or or anything in between.”

It’s still possible that trade-offs take place at the level of genus, Mason said, or that they influence species relatively fleetingly as evolutionary pressures appear and disappear.

But as a broad effect on an entire family of birds, a voice–plumage trade off doesn’t seem to exist. One possibility is that the resources needed to develop fancy plumage are different from the ones required for complex songs, freeing tanagers to invest in both forms of showiness simultaneously.

“No other part of Darwin’s childhood home is accessible to the public, so when we were offered the chance to buy this slip of woodland next to the river, we were thrilled at the opportunity to open up a cherished corner of his world,” said Colin Preston, Director of Shropshire Wildlife Trust.

While much of the land previously attached to The Mount, his birthplace, has disappeared under housing, other parts survived in private gardens, including the land the Trust has bought.

Through the wood, alongside an ice house once used by the Darwins, runs a path with views down to the River Severn. It was here 200 years ago, that the young Darwin was sent every day before breakfast to walk the path at the bottom of the garden. It was known as the Thinking Path and provided a regular time for thought and reflection. The habit became ingrained in Darwin’s daily routine and when he and his wife Emma bought Down House in Kent, they made their own Sandwalk through the grounds, carrying on the tradition of morning walks with their children.

The Trust intends to restore the Thinking Path, open up views and carry out essential boundary and safety work. The garden will be opened for group visits at various times throughout the year and schoolchildren will have the chance to walk in Darwin’s footsteps, inspiring them to enjoy and explore the natural world.

Several studies and unpublished reports have shown that particular species are more approachable on islands where there are fewer predators, or quicker to flee on islands that contain introduced hunters such as feral cats. But despite this largely anecdotal evidence for island tameness, “no one has ever established that it’s a general phenomenon in any group”, says Cooper. “We showed that for a large prey group — lizards — there really is a significant decline in wariness on islands.”

Taming of the few

“Island tameness is an old idea, but there have been few tests of it,” says Dan Blumstein, a behavioural biologist at the University of California, Los Angeles. “This is a needed paper that convincingly shows some of the drivers of island tameness in lizards.”

Cooper and his colleagues scoured past studies and collated data on the distance at which lizards start to flee when approached by a researcher. They took a conservative approach, discarding studies in which researchers had pointed at the lizards, walked towards the animals faster or slower than a particular fixed speed, or studied populations that were habituated to humans.

Cooper and his team ended up with data for 66 species, from the Eurasian common lizard (Zootoca vivipara) to the Galapagos marine iguana (Amblyrhynchus cristatus). The results clearly showed that humans can get closer to island-dwelling lizards than to mainland ones, and that lizards become more approachable on islands that are farther from the mainland.

Island ecology is so important that it overrides any effect of evolutionary history, Cooper and his co-authors say. They also showed that even closely related lizard species have different escape behaviours depending on where they live, and that their evolutionary relationships were mostly irrelevant.

The results do not explain why island lizards are tamer than those on the mainland, although the relative lack of island predators is the most likely reason. Animals with skittish dispositions can needlessly abandon valuable resources, and natural selection would be expected to weed out such responses if predators are rare or absent.

Cooper wants to test this idea, but says that it is hard to get decent data on the numbers, densities and types of predators on different islands.

Darwin went on to become extremely wealthy by careful dealing in the stocks and shares of the developing railway system.

None of this should be seen as reducing Darwin’s status as a scientist, nor as a humanitarian – he was anti-slavery and anti-racist – but out of the pair Wallace is arguably the more intriguing.

Not only did he discover the mechanism of evolutionary change, he was a prominent advocate of the socialist ideas that were then occupying the thoughts of a German economist named Karl Marx and English mill-owner Robert Owen and also campaigned for the public ownership of land.

So this year’s celebrations of the centenary of Wallace’s death are not to be missed.

A team of enthusiasts and scientists are running a programme of lectures and events centred around the Natural History Museum, but also incorporating a range of venues across the country.

A talk on June 6 at the museum is the next opportunity to discover more about this great thinker.

This fifth talk, titled Making Livings: Why Darwin’s and Wallace’s Theories Were Worlds Apart, will “explore how different the Victorian naturalists … were in their socio-economic backgrounds and in their thinking about evolution.”

Even comedian Bill Bailey has been getting involved in the centenary project, describing Wallace as “the greatest field naturalist of the 19th century – perhaps ever.”

Indeed, he is such a fan that he produced a pair of recent TV programmes on the scientist, in which he points out that “a huge swathe of Indonesia,” where Wallace carried out much of his research, “is named after the great man himself” – the 350,000 square kilometres of Wallacea.

To date, it seems that Indonesia has more respect for this evolutionary titan than has his homeland.

Admission to the Natural History Museum talk is free, but seats must be booked via the museum’s website at www.nhm.ac.uk.

Wallace came from a lower middle-class background. His father was a provincial solicitor, at that time a lowly occupation. He left school at 14 to work as an apprentice railway surveyor with his brother William in order to supplement the family income.

While working on the railways Wallace talked of being forced to travel in the “wretched third-class” carriages where passengers in open trucks were transported like cattle.

After one such journey with his brother William they took cheap lodgings in a damp room in Bristol, which led to his brother dying of pneumonia.

Wallace’s mental development was grounded in the provincial, industrialising countryside, where he would mix with weavers, factory inspectors, railway workers and farm labourers.

He was completely self-educated in the sciences and became an early socialist, greatly influenced by lectures he heard in the Hall of Science in Tottenham Court Road given by Robert Owen.

“I have always looked upon Owen as my first teacher in the philosophy of human nature and my first guide through the labyrinth of social science.”

He, like Owen, took a prominently anti-Malthusian line – put crudely, Malthus argued that disease and early death were necessary among the working masses to keep the population down.

Although his family was “old-fashioned Church of England” Wallace very soon shed all shreds of religiosity, developing advanced secular views on society and human nature.

Ironically, because of his radical political views Wallace was from the outset a more likely candidate than Darwin to come up with such a radical hypothesis as evolution.

But he undoubtedly lacked the self-confidence that comes with a public-school education and affluence.

In 1847 Bates and Wallace discussed travelling abroad and earning their living collecting specimens along the River Amazon.

Unlike Darwin, who was easily able to organise and finance his own long voyage on the Beagle, Wallace and Bates had to beg money for their trip. The mania of Victorians for collecting natural history specimens gave them the opportunity.

In 1848 the pair were able to sail for Brazil, where they spent several years enduring disease, hardship and catastrophe.

Their experiences were physically as far removed from Darwin’s relaxed and comfortable Beagle voyage as could be imagined. Unfortunately Wallace’s return voyage ended in shipwreck and the loss of all his meticulously recorded notes and arduously collected specimens.

In 1853, despite vowing never again to return to sea, Wallace again set sail, this time for Malaysia, with the same aims as before in the Amazon.

He also wished to investigate local tribes and pursue his ideas on human origins. His readings of the anonymously published book Vestiges of the Natural History of Creation had convinced him that humans were descended from apes, possibly from an orang-utan-like animal as found in Malaysia.

Before he left he dispatched a short theoretical paper that Darwin and his friends Edward Blyth and the renowned geologist Charles Lyell read, in which he speculated about how varieties of species arise and how geography was key in determining origins.

His sponsors felt he should not waste his time with such pointless speculation and concentrate on obtaining specimens for their collections.

However, Darwin wrote him a warm and encouraging letter complimenting him on his paper. In 1858, after a bad bout of malaria, Wallace wrote another paper setting out for the first time his basic idea of natural selection and evolutionary development. He was completely unaware that Darwin had been secretly working along similar lines.

He sent it to Darwin and asked the latter to forward it to Lyell. The way his seminal paper overlapped with Darwin’s thinking on the same issue was remarkable.

Darwin had also collected a mass of fascinating data during his trip on the Beagle and through diligent correspondence with other naturalists was developing his own draft ideas of evolution.

Wallace’s paper, arriving out of the blue, hit him like a thunderbolt. He’d fleetingly met and then corresponded with Wallace but the two men hardly knew each other.

Darwin was aghast and shattered that someone had apparently beaten him to it. The idea of “losing” the letter or ignoring it crossed his mind – but in the end he followed the honourable road and forwarded it to his friend, the renowned geologist Lyell, as Wallace had requested.

Darwin was, in fact, about to write to Wallace congratulating him and had almost decided to throw in the towel on his own projected publication, but was dissuaded from doing so by botanist Joseph Hooker and Lyell.

Darwin felt he no longer had the right to publish his own views before Wallace’s now he had read the latter’s paper. But Hooker and Lyell persuaded him to publish a paper of his own alongside Wallace’s in the Journal of the Linnaean Society.

As he was a renowned fellow of the society, Lyell and Hooker knew Darwin’s piece would take precedence over that of the “mere collector” Wallace, who lacked standing in scientific circles.

Wallace, unlike Darwin, had no independent means, was not a member of the gentry nor was he university educated.

Darwin and his colleagues viewed Wallace as a useful purveyor of information and specimens, but would not have considered him a philosopher or thinker on their own level. That was partly why Wallace’s paper hit them with such force.

Neither paper caused even a ripple of excitement or outrage at the time of publication, but Darwin, realising the danger to his own work if Wallace developed his ideas further, put his head down and worked like a man possessed to finish and publish his later world-renowned On the Origin of Species a year later in 1859.

This was the book that shook the world. Priests began apoplectically raging from their pulpits, fine ladies had fainting fits at the idea of being related to monkeys and the popular papers never tired of ridiculing the idea of evolution as if a new flat-earth theory were being propounded.

These historical events demonstrate how class invariably determine an individual’s fortune and later historical status.

The strictly stratified Victorian society left Wallace little chance of entering the hallowed halls of the elite scientific community of which Darwin was already a respected member.

However, after his return from his travels and with generous support from Darwin, he did eventually gain acceptance, becoming a revered member of those circles.

Wallace had to establish his reputation the hard way, but humble and modest as ever he subsequently accepted Darwin’s pre-eminence and his own secondary role in developing the theory of evolution. Undoubtedly Wallace deserves more prominence than history has granted him.

A display to commemorate the centenary of Alfred Russel Wallace’s death opened this week at the archives reading room at Kew Gardens and runs until May 20. For more information about further commemorative events around the country visit the Natural History Museum website (www.nhm.ac.uk).